Molecular Ecology (2012) 21, 4663–4664
NEWS AND VIEWS
PERSPECTIVE
Illegal gene flow from transgenic
creeping bentgrass: the saga continues
ALLISON A. SNOW
Department of Evolution, Ecology, and Organismal Biology, The
Ohio State University, Columbus, OH 43210, USA
Ecologists have paid close attention to environmental
effects that fitness-enhancing transgenes might have following crop-to-wild gene flow (e.g. Snow et al. 2003). For
some crops, gene flow also can lead to legal problems,
especially when government agencies have not approved
transgenic events for unrestricted environmental release.
Creeping bentgrass (Agrostis stolonifera), a common turfgrass used in golf courses, is the focus of both areas of
concern. In 2002, prior to expected deregulation (still
pending), The Scotts Company planted creeping bentgrass with transgenic resistance to the herbicide glyphosate, also known as RoundUp, on 162 ha in a
designated control area in central Oregon (Fig. 1).
Despite efforts to restrict gene flow, wind-dispersed pollen carried transgenes to florets of local A. stolonifera
and A. gigantea as far as 14 km away, and to sentinel
plants placed as far as 21 km away (Watrud et al. 2004).
Then, in August 2003, a strong wind event moved transgenic seeds from windrows of cut bentgrass into nearby
areas. The company’s efforts to kill all transgenic survivors in the area failed: feral glyphosate-resistant populations of A. stolonifera were found by Reichman et al.
(2006), and 62% of 585 bentgrass plants had the telltale
CP4 EPSPS transgene in 2006 (Zapiola et al. 2008; Fig. 2).
Now, in this issue, the story gets even more interesting
as Zapiola & Mallory-Smith (2012) describe a transgenic,
intergeneric hybrid produced on a feral, transgenic creeping bentgrass plant that received pollen from Polypogon
monspeliensis (rabbitfoot grass). Their finding raises a
host of new questions about the prevalence and fitness of
intergeneric hybrids, as well as how to evaluate the full
extent of gene flow from transgenic crops.
To date, only a few other cases of spontaneous gene flow
from transgenic crops to wild, weedy, or feral populations
have been reported (e.g. Hall et al. 2000; Warwick et al.
2008; Schafer et al. 2011), although others are likely to follow when more species of transgenic crops are released
near compatible relatives. For example, transgenic rice has
been cultivated near weedy rice in the USA and China
(where it is still regulated), and genetically engineered
traits are expected to spread to conspecific weedy rice populations (Yang et al. 2011).
During 2003–2006, Zapiola et al. (2008) screened hundreds of in situ bentgrass plants and thousands of their
progeny to test for glyphosate resistance. A glyphosateresistant plant found inside the control area in 2005 produced a transgenic seedling that appeared to be a hybrid.
Using a combination of nuclear and maternally inherited
DNA markers, the authors identified this ‘off-type’ seedling as an intergeneric hybrid with rabbitfoot grass. The F1
Fig. 1 Creeping bentgrass and rabbitfoot grass occur along
canals and irrigation ditches within the designated control area
near Madras, Oregon. Photo courtesy of M. L. Zapiola.
Keywords: feral, gene flow, genetically modified organisms,
hybridization, naturalized
Received 24 April 2012; revision received 26 May 2012; accepted
4 June 2012
Correspondence: Allison Snow, Fax: 614-292-2070;
E-mail: [email protected]
2012 Blackwell Publishing Ltd
Fig. 2 A feral, glyphosate-resistant creeping bentgrass plant
established along a ditch within the control area. Photo courtesy of M. L. Zapiola.
4664 N E W S A N D V I E W S : P E R S P E C T I V E
hybrid produced stolons, flowered without vernalization,
and produced 14 viable seeds from 90 florets in bagged
panicles. The current Agrostis study is noteworthy because:
1 This is the first report of spontaneous gene flow resulting in a transgenic, intergeneric hybrid;
2 It is a clear example of the otherwise poorly understood
extent of spontaneous hybridization in Agrostis and
Polypogon spp.;
3 In this context, herbicide resistance from a known transgenic event (ASR368) provided a powerful method for
tracking and understanding gene flow in the Agrostis
complex;
4 The study provides valuable information regarding gene
flow in a naturalized, non-native, perennial, outcrossing
species that is considered to be a weed in some crops
and nonagricultural habitats in the USA and elsewhere;
and
5 These results question the efficacy of the stringent procedures put in place for preventing unintended gene flow
from field trials of regulated transgenic plants.
Public-sector researchers have been very resourceful in taking advantage of this ‘natural experiment’ in the face of
miss-steps and ongoing eradication efforts by The Scotts
Company.
Previously, Monsanto Company and Scotts had
described the potential for intergeneric hybrids with rabbitfoot grass in a petition to USDA for nonregulated status
(Frelich et al. 2003), stating that ‘on the rare occasions that
hybrids have been noted, the hybrids have been sterile
(Björkman 1960)’. Low fertility is common in hybrids and
is not surprising here given that creeping bentgrass and
rabbitfoot grass have different chromosome numbers.
However, spontaneous backcrossing and ⁄ or loss of extraneous chromosomes has been shown to restore fertility in
other crop-wild systems, including intergeneric hybrids
between winter wheat (Triticum aestivum) and weedy
jointed goatgrass (Aegilops cylindrica) (e.g. Perez-Jones et al.
2010 and references therein). In fact, jointed goatgrass was
able to acquire a mutation-derived gene for resistance to
imazamox, an imidazolinone herbicide, from wheat in a
commercial field in Oregon. Brassica napus (canola) and
weedy B. rapa also have different chromosome numbers
but transgenes have been shown to introgress into diploid
B. rapa following spontaneous hybridization in Canada
(Warwick et al. 2008). A logical next step for the bentgrass
system is to create advanced-generation intergeneric
hybrids to study their mating system, ploidy, fitness and
competitive ability, and to include P. monspeliensis in
future risk assessments.
In summary, the saga of Roundup Ready creeping
bentgrass offers valuable lessons about how to prevent the
escape of regulated transgenes via pollen, seeds and vegetative propagules. Scotts Company was fined $500 000 in
2007 for allowing regulated transgenes to escape, perhaps
irretrievably. Meanwhile, in October 2010, the presence of
transgenic creeping bentgrass was confirmed in a new area
in eastern Oregon, directly across the state border from
field trials that were carried out by the Scotts Company in
Idaho (Mallory-Smith 2011). Further studies should examine whether the ongoing and accidental spread of glyphosate-resistant
perennial
grasses
represents
an
environmental and ⁄ or economic concern and, if so, how to
address it.
References
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Frelich J, Huber S, Nelson E, Stone T (2003) Petition for determination of nonregulated status of Roundup Ready creeping bentgrass (Agrostis stolonifera L.) event ASR368 for determination of
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2012 Blackwell Publishing Ltd